Calcium spike and calcium-dependent potassium conductance in mechanosensory neurons of the lamprey.

Abstract

Action potentials (APs) of long duration (up to 1 s) followed by prolonged (0.5-5 s) hyperpolarizing afterpotentials (HAP) were recorded in lamprey primary mechanosensory neurons (dorsal cells) in isolated spinal cords exposed to either or both of the potassium channel blockers, tetrathylammonium (TEA) and 3,4-diaminopyridine (DAP). The membrane events underlying the prolonged AP and HAP were investigated in current clamp studies and were shown to be a Ca spike- and a Ca-dependent K conductance, respectively. The prolonged AP was accompanied by an increased membrane conductance and, unlike the normal Na AP in these cells, was not blocked by tetrodotoxin (TTX) or by replacement of external Na with choline or TEA. Reduction of [Ca]o from 10 to 0 mM reduced the amplitude and duration of the prolonged TTX-resistant AP but did not eliminate it within the 15-min washout period, probably because of Ca buffering in the spinal cord. The overshoot of the prolonged AP varied in amplitude as a linear function of the log of the external Ca concentration (2.5-10 mM) with a slope of 31.5 mV for a 10-fold change in Ca concentration, a value close to the 28 mV expected from the Nernst relation. Co (2 mM) and Cd (1 mM) blocked the prolonged APs. Ba and Sr substituted for Ca. The APs in Ba were extremely long lasting (up to 40 s). The HAPs following Ca spikes were 0.5-5 s in duration (peak to half amplitude) and were accompanied by an increased membrane conductance. The HAP varied in amplitude with the extracellular K concentration, reversed in sign at the presumed K equilibrium potential (-90 mV), and was insensitive to injected Cl. We conclude that HAP is a result of increased K conductance. The increase in K conductance during the HAP appeared to be dependent on Ca influx, because the amplitude and duration of the HAP varied with the extracellular Ca concentration and increased in duration during repetitive Ca spike activation, presumably as a result of accumulation of Ca intracellularly. Further, the HAP was absent following even very long lasting spikes in Ba, an ion that in other cells does not activate the Ca-dependent K conductance. Small regenerative depolarizations sometimes followed Ca spikes in dorsal cell somata. These are believed to reflect Ca spikes in discrete axonal regions at various electrotonic distances from the soma.